Interaction between nitric oxide synthase inhibitor induced oscillations and the activation flow coupling response

The role of nitric oxide (NO) in the activation-flow coupling (AFC) response to periodic electrical forepaw stimulation was investigated using signal averaged laser Doppler (LD) flowmetry. LD measures of calculated cerebral blood flow (CBF) were obtained both prior and after intra-peritoneal administration of the non-selective nitric oxide synthase (NOS) inhibitor, N(G)-nitro-L-arginine (L-NNA) (40 mg/kg). Characteristic baseline low frequency vasomotion oscillations (0.17 Hz) were observed after L-NNA administration. These LD(CBF) oscillations were synchronous within but not between hemispheres. L-NNA reduced the magnitude of the AFC response (p<0.05) for longer stimuli (1 min) with longer inter-stimulus intervals (2 min). In contrast, the magnitude of the AFC response for short duration stimuli (4 s) with short inter-stimulus intervals (20 s) was augmented (p<0.05) after L-NNA. An interaction occurred between L-NNA induced vasomotion oscillations and the AFC response with the greatest increase occurring at the stimulus harmonic closest to the oscillatory frequency. Nitric oxide may therefore modulate the effects of other vasodilators involved in vasomotion oscillations and the AFC response.

[1]  D J Reis,et al.  Vasodilation evoked from medulla and cerebellum is coupled to bursts of cortical EEG activity in rats. , 1995, The American journal of physiology.

[2]  A. Villringer,et al.  Role of nitric oxide in the coupling of cerebral blood flow to neuronal activation in rats , 1993, Neuroscience Letters.

[3]  P. Moore,et al.  Selective inhibitors of neuronal nitric oxide synthase--is no NOS really good NOS for the nervous system? , 1997, Trends in pharmacological sciences.

[4]  C. Iadecola,et al.  Permissive and obligatory roles of NO in cerebrovascular responses to hypercapnia and acetylcholine. , 1996, The American journal of physiology.

[5]  S. Yang,et al.  Nitric oxide of neuronal origin mediates NMDA‐induced cerebral hyperemia in rats , 1998, Neuroreport.

[6]  O. Inanami,et al.  Nitric oxide (NO) is involved in increased cerebral cortical blood flow following stimulation of the nucleus basalis of Meynert in anesthetized rats , 1992, Neuroscience Letters.

[7]  R. Berne,et al.  Competitive inhibition of nitric oxide synthase prevents the cortical hyperemia associated with peripheral nerve stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Zoltán Benyó,et al.  The cerebrocortical microcirculatory effect of nitric oxide synthase blockade is dependent upon baseline red blood cell flow in the rat , 2000, Neuroscience Letters.

[9]  M. Stern,et al.  In vivo evaluation of microcirculation by coherent light scattering , 1975, Nature.

[10]  A Villringer,et al.  Coupling of cerebral blood flow to neuronal activation: role of adenosine and nitric oxide. , 1994, The American journal of physiology.

[11]  M. Lauritzen,et al.  Laser-Doppler Evaluation of Rat Brain Microcirculation: Comparison with the [14C]-Iodoantipyrine Method Suggests Discordance during Cerebral Blood Flow Increases , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[12]  L. Sokoloff,et al.  Increases in local cerebral blood flow associated with somatosensory activation are not mediated by NO. , 1994, The American journal of physiology.

[13]  M. Moskowitz,et al.  L-NA-Sensitive rCBF Augmentation during Vibrissal Stimulation in Type III Nitric Oxide Synthase Mutant Mice , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[14]  A Villringer,et al.  Nitric oxide synthase blockade enhances vasomotion in the cerebral microcirculation of anesthetized rats. , 1993, Microvascular research.

[15]  John A Detre,et al.  Transcranial laser doppler mapping of activation flow coupling of the rat somatosensory cortex , 1998, Neuroscience Letters.

[16]  K Messmer,et al.  Spontaneous arteriolar vasomotion as a determinant of peripheral vascular resistance. , 1983, International journal of microcirculation, clinical and experimental.

[17]  D. Heistad,et al.  Vasomotion of basilar arteries in vivo. , 1990, The American journal of physiology.

[18]  M. Moskowitz,et al.  Regional cerebral blood flow response to vibrissal stimulation in mice lacking type I NOS gene expression. , 1996, The American journal of physiology.

[19]  C. Szabó Physiological and pathophysiological roles of nitric oxide in the central nervous system , 1996, Brain Research Bulletin.

[20]  J O Skarphedinsson,et al.  Repeated measurements of cerebral blood flow in rats. Comparisons between the hydrogen clearance method and laser Doppler flowmetry. , 1988, Acta physiologica Scandinavica.

[21]  T. Ebner,et al.  Nitric oxide is the predominant mediator of cerebellar hyperemia during somatosensory activation in rats. , 1999, The American journal of physiology.

[22]  P. Magistretti,et al.  Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[23]  Alan P. Koretsky,et al.  BOLD fMRI and somatosensory evoked potentials are well correlated over a broad range of frequency content of somatosensory stimulation of the rat forepaw , 2008, Brain Research.

[24]  Thomas T. Liu,et al.  An arteriolar compliance model of the cerebral blood flow response to neural stimulus , 2005, NeuroImage.

[25]  R. Koehler,et al.  Interaction of nitric oxide, 20-HETE, and EETs during functional hyperemia in whisker barrel cortex. , 2008, American journal of physiology. Heart and circulatory physiology.

[26]  A. Hudetz,et al.  Modification of cerebral laser-Doppler flow oscillations by halothane, PCO2, and nitric oxide synthase blockade. , 1995, The American journal of physiology.

[27]  K. Breese,et al.  Nitric oxide mediates vasodilatation in response to activation of N-methyl-D-aspartate receptors in brain. , 1993, Circulation research.

[28]  Elliot A. Stein,et al.  Anesthesia alters NO-mediated functional hyperemia , 2001, Brain Research.

[29]  R L Haberl,et al.  Laser-Doppler assessment of brain microcirculation: effect of systemic alterations. , 1989, The American journal of physiology.

[30]  B B Biswal,et al.  Synchronous oscillations in cerebrocortical capillary red blood cell velocity after nitric oxide synthase inhibition. , 1996, Microvascular research.

[31]  I. Kanno,et al.  Effect of nitric oxide synthase inhibitor on the local cerebral blood flow evoked by rat somatosensory stimulation under hyperoxia. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[32]  W H Schuette,et al.  Low-Frequency Oscillations of Cortical Oxidative Metabolism in Waking and Sleep , 1988, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[33]  M. Ursino,et al.  Theoretical analysis of complex oscillations in multibranched microvascular networks. , 1996, Microvascular research.

[34]  P A Flecknell,et al.  A comparison of measurements of cerebral blood flow in the rabbit using laser Doppler spectroscopy and radionuclide labelled microspheres. , 1988, Clinical physics and physiological measurement : an official journal of the Hospital Physicists' Association, Deutsche Gesellschaft fur Medizinische Physik and the European Federation of Organisations for Medical Physics.

[35]  C. N. Guy,et al.  fMRI and EEG Responses to Periodic Visual Stimulation , 1999, NeuroImage.

[36]  J. Mayhew,et al.  Fine detail of neurovascular coupling revealed by spatiotemporal analysis of the hemodynamic response to single whisker stimulation in rat barrel cortex. , 2008, Journal of neurophysiology.

[37]  J. Mayhew,et al.  Cerebral Vasomotion: A 0.1-Hz Oscillation in Reflected Light Imaging of Neural Activity , 1996, NeuroImage.

[38]  T. Griffith,et al.  Temporal chaos in the microcirculation. , 1996, Cardiovascular research.

[39]  R J Roman,et al.  Spontaneous Flow Oscillations in the Cerebral Cortex during Acute Changes in Mean Arterial Pressure , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[40]  U. Dirnagl,et al.  Continuous Measurement of Cerebral Cortical Blood Flow by Laser—Doppler Flowmetry in a Rat Stroke Model , 1989, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[41]  A. Ngai,et al.  L-NNA suppresses cerebrovascular response and evoked potentials during somatosensory stimulation in rats. , 1995, The American journal of physiology.

[42]  R. Koehler,et al.  Dependency of Cortical Functional Hyperemia to Forepaw Stimulation on Epoxygenase and Nitric Oxide Synthase Activities in Rats , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[43]  M. Lauritzen,et al.  NOS activity in brain and endothelium: relation to hypercapnic rise of cerebral blood flow in rats. , 1996, The American journal of physiology.

[44]  E. Bouskela,et al.  Inhibition of Nitric Oxide Synthase Attenuates the Cerebral Blood Flow Response to Stimulation of Postganglionic Parasympathetic Nerves in the Rat , 1993, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[45]  U Dirnagl,et al.  Nitric oxide: a modulator, but not a mediator, of neurovascular coupling in rat somatosensory cortex. , 1999, The American journal of physiology.

[46]  H. Wiesinger Arginine metabolism and the synthesis of nitric oxide in the nervous system , 2001, Progress in Neurobiology.

[47]  D. Leibfritz,et al.  Free radicals and antioxidants in normal physiological functions and human disease. , 2007, The international journal of biochemistry & cell biology.

[48]  K A Easley,et al.  Cortical cerebral blood flow cycling: anesthesia and arterial blood pressure. , 1995, The American journal of physiology.

[49]  A Villringer,et al.  Coupling of brain activity and cerebral blood flow: basis of functional neuroimaging. , 1995, Cerebrovascular and brain metabolism reviews.

[50]  M Intaglietta,et al.  Evidence of flowmotion induced changes in local tissue oxygenation. , 1993, International journal of microcirculation, clinical and experimental.

[51]  Giuseppe Baselli,et al.  Coupling arterial windkessel with peripheral vasomotion: modeling the effects on low-frequency oscillations , 2006, IEEE Transactions on Biomedical Engineering.

[52]  A. Villringer,et al.  Spontaneous Low Frequency Oscillations of Cerebral Hemodynamics and Metabolism in Human Adults , 2000, NeuroImage.

[53]  M. Moskowitz,et al.  Nitric Oxide Synthase Inhibition and Cerebrovascular Regulation , 1994, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[54]  Angelo Gemignani,et al.  Pial arteriolar vasomotion changes during cortical activation in rats , 2007, NeuroImage.